CHIP suppresses the proliferation and migration of A549 cells by mediating the ubiquitination of eIF2α and upregulation of tumor suppressor RBM5

J Biol Chem. 2024 Mar;300(3):105673. doi: 10.1016/j.jbc.2024.105673. Epub 2024 Jan 23.

Abstract

The protein kinase RNA-like endoplasmic reticulum kinase (PERK)-eukaryotic translation initiation factor 2 subunit α (eIF2α) pathway plays an essential role in endoplasmic reticulum (ER) stress. When the PERK-eIF2α pathway is activated, PERK phosphorylates eIF2α (p-eIF2α) at Ser51 and quenches global protein synthesis. In this study, we verified eIF2α as a bona fide substrate of the E3 ubiquitin ligase carboxyl terminus of the HSC70-interaction protein (CHIP) both in vitro and in cells. CHIP mediated the ubiquitination and degradation of nonphosphorylated eIF2α in a chaperone-independent manner and promoted the upregulation of the cyclic AMP-dependent transcription factor under endoplasmic reticulum stress conditions. Cyclic AMP-dependent transcription factor induced the transcriptional enhancement of the tumor suppressor genes PTEN and RBM5. Although transcription was enhanced, the PTEN protein was subsequently degraded by CHIP, but the expression of the RBM5 protein was upregulated, thereby suppressing the proliferation and migration of A549 cells. Overall, our study established a new mechanism that deepened the understanding of the PERK-eIF2α pathway through the ubiquitination and degradation of eIF2α. The crosstalk between the phosphorylation and ubiquitination of eIF2α shed light on a new perspective for tumor progression.

Keywords: CHIP; ER stress; PERK; RBM5; eIF2; phosphorylation; protein degradation; ubiquitination.

MeSH terms

  • A549 Cells
  • Cell Movement / genetics
  • Cell Proliferation / genetics
  • Cyclic AMP / metabolism
  • Endoplasmic Reticulum Stress / genetics
  • Eukaryotic Initiation Factor-2* / genetics
  • Eukaryotic Initiation Factor-2* / metabolism
  • Genes, Tumor Suppressor*
  • Humans
  • Phosphorylation
  • Transcription Factors / metabolism
  • Ubiquitin-Protein Ligases* / metabolism
  • Ubiquitination* / genetics
  • Up-Regulation* / genetics

Substances

  • Cyclic AMP
  • Eukaryotic Initiation Factor-2
  • Transcription Factors
  • EIF2AK3 protein, human
  • EIF2S1 protein, human
  • RBM5 protein, human
  • Ubiquitin-Protein Ligases